The essential role of clathrin-mediated endocytosis in yellow head virus propagation in the black tiger shrimp Penaeus monodon

Developmental and Comparative Immunology

Volumn 44, Issue 1, 2014, Pages 100-110

  Jatuyosporn, Thapanan ^a   Supungul, Premruethai ^a,b   Tassanakajon, Anchalee ^a   Krusong, Kuakarun ^a  

^a CHULALONGKORN UNIVERSITY   (Thailand)

^b NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

Author keywords

AP17; Clathrin coat assembly protein 17; Clathrin mediated endocytosis; Penaeus monodon; Pm; Yellow head virus; YHV

Indexed keywords

ASSEMBLY PROTEIN 17; CHLORPROMAZINE; CLATHRIN ASSEMBLY PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; AP17 GENE; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; GENE SILENCING; IMMUNOFLUORESCENCE MICROSCOPY; MICROARRAY ANALYSIS; NIDOVIRALES; NIDOVIRALES INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PENAEUS MONODON; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SEQUENCE ALIGNMENT; TISSUE DISTRIBUTION; VIRUS ENTRY; VIRUS REPLICATION; YELLOW HEAD VIRUS; YELLOW HEAD VIRUS INFECTION;

DECAPODA (CRUSTACEA); PENAEUS MONODON; YELLOW HEAD VIRUS;

CLATHRIN COAT ASSEMBLY PROTEIN 17; CLATHRIN-MEDIATED ENDOCYTOSIS; PENAEUS MONODON; YELLOW HEAD VIRUS; YHV;

ADAPTOR PROTEIN COMPLEX 2; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELLS, CULTURED; CHLORPROMAZINE; CLATHRIN; CYTOPLASM; ENDOCYTOSIS; HEMOCYTES; NIDOVIRALES INFECTIONS; PENAEIDAE; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; RONIVIRIDAE; UP-REGULATION; VIRUS REPLICATION;

EID: 84891049540     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2013.11.017     Document Type: Article

References (56)

1. Aguilar R.C., Ohno H., Roche K.W., Bonifacino J.S. Functional domain mapping of the clathrin-associated adaptor medium chains mu1 and mu2. J. Biol. Chem. 1997, 272(43):27160-27166.
2. Ahle S., Mann A., Eichelsbacher U., Ungewickell E. Structural relationships between clathrin assembly proteins from the golgi and the plasma membrane. EMBO. J. 1988, 7(4):919-929.
3. Alonso C., Galindo I., Cuesta-Geijo M.A., Cabezas M., Hernaez B., Munoz-Moreno R. African swine fever virus-cell interactions: from virus entry to cell survival. Virus Res. 2013, 173(1):42-57.
4. Assavalapsakul W., Smith D.R., Panyim S. Identification and characterization of a Penaeus monodon lymphoid cell-expressed receptor for the yellow head virus. J. Virol. 2006, 80(1):262-269.
5. Assavalapsakul W., Tirasophon W., Panyim S. Antiserum to the gp116 glycoprotein of yellow head virus neutralizes infectivity in primary lymphoid organ cells of Penaeus monodon. Dis. Aquat. Organ. 2005, 63(1):85-88.
6. Bartosch B., Cosset F.L. Cell entry of hepatitis C virus. Virology 2006, 348(1):1-12.
7. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: Signalp 3.0. J. Mol. Biol. 2004, 340(4):783-795.
8. Bernardes C., Antonio A., Pedroso de Lima M.C., Valdeira M.L. Cholesterol affects African swine fever virus infection. Biochim. Biophys. Acta 1998, 1393(1):19-25.
9. Blanchard E., Belouzard S., Goueslain L., Wakita T., Dubuisson J., Wychowski C., Rouille Y. Hepatitis C virus entry depends on clathrin-mediated endocytosis. J. Virol. 2006, 80(14):6964-6972.
10. Chantanachookin C.S., Boonyaraypalin J., Kasornchnadra S., Direkbusarakorm U., Ekpanithanpong K., Supamataya S., Sriurairatana T., Flegel W. Histologu and ultrastructure reveal a new granulosis-like virus in Penaeus monodon affected by yellowhead disease. Dis. Aquat. Organ. 1993, 17:145-157.
11. Chen Y., Maguire T., Hileman R.E., Fromm J.R., Esko J.D., Linhardt R.J., Marks R.M. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 1997, 3(8):866-871.
12. Chou T. Stochastic entry of enveloped viruses: fusion versus endocytosis. Biophys. J. 2007, 93(4):1116-1123.
13. Chu J.J., Leong P.W., Ng M.L. Analysis of the endocytic pathway mediating the infectious entry of mosquito-borne flavivirus West Nile into Aedes albopictus mosquito (C6/36) cells. Virology 2006, 349(2):463-475.
14. Cole C., Barber J.D., Barton G.J. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 2008, 36:W197-201. (Web Server issue).
15. Crowther R.A., Finch J.T., Pearse B.M. On the structure of coated vesicles. J. Mol. Biol. 1976, 103(4):785-798.
16. Diaz-Griffero F., Jackson A.P., Brojatsch J. Cellular uptake of avian leukosis virus subgroup B is mediated by clathrin. Virology 2005, 337(1):45-54.
17. Dimitrov D.S. Virus entry: molecular mechanisms and biomedical applications. Nat. Rev. Microbiol. 2004, 2(2):109-122.
18. Flegel T.W. Special topic review: major viral diseases of the black tiger prawn (Penaeus monodon) in Thailand. World J. Microbiol. Biotechnol. 1997, 13:433-442.
19. Gasteiger E., Hoogland C., Gattiker A., Duvaud S., Wilkins M.R., Appel R.D., Bairoch A. Protein identification and analysis tools on the ExPASy server. The Proteomics Protocols Handbook 2005, 571-607. Springer, Humana Press. J.M. Walker (Ed.).
20. Husain M., Moss B. Role of receptor-mediated endocytosis in the formation of vaccinia virus extracellular enveloped particles. J. Virol. 2005, 79(7):4080-4089.
21. Jitrapakdee S., Unajak S., Sittidilokratna N., Hodgson R.A., Cowley J.A., Walker P.J., Panyim S., Boonsaeng V. Identification and analysis of gp116 and gp64 structural glycoproteins of yellow head nidovirus of Penaeus monodon shrimp. J. Gen. Virol. 2003, 84(Pt 4):863-873.
22. Kiatpathomchai W., Jitrapakdee S., Panyim S., Boonsaeng V. RT-PCR detection of yellow head virus (YHV) infection in Penaeus monodon using dried haemolymph spots. J. Virol. Met. 2004, 119(1):1-5.
23. Kim C., Bergelson J.M. Echovirus 7 entry into polarized intestinal epithelial cells requires clathrin and Rab7. MBio 2012, 3(2):1-10.
24. Lightner D.V., Hasson K.W., Whiye B.L., Redman R.M. Experimental infection of Western hemisphere penaeid shrimp with Asian white spot syndrome virus and Asian yellowhead virus. J. Aquat. Anim. Health 1998, 10:271-281.
25. Limsuwan C. Handbook for Cultivation of Black Tiger Prawns 1991, Tansetakit, Bangkok, Thailand.
26. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25(4):402-408.
27. Lu Y., Tapay L.M., Brock J.A., Loh P.C. Infection of the yellowhead baculo-like virus (YBV) in two species of penaeid shrimp, Penaeus stylirostris (Simpson) and Penaeus vannamei (Boone). J. Fish. Dis. 1994, 17:649-656.
28. Lu Y., Tapay L.M., Gose R.B., Brock J.A., Loh P.C. Infectivity of yellowhead virus (YHV) and the Chinese baculo-like virus (CBV) in two species of penaeid shrimp, Penaeus stylirostris (Stimpson) and Penaeus vannamei (Boone). Diseases in Asian Aquaculture III 1997, Asian Fisheries Society, Manila, Philippine. F.W. Flegel, I.H. MacRae (Eds.).
29. Lu Y., Tapay L.M., Loh P.C., Brock J.A., Gose R.B. Distribution of yellow head virus in selected tissue and organs of penaeid shrimp Penaeus vannamei. Dis. Aquat. Organ. 1995, 23:67-70.
30. Meier O., Boucke K., Hammer S.V., Keller S., Stidwill R.P., Hemmi S., Greber U.F. Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J. Cell. Biol. 2002, 158(6):1119-1131.
31. Meier O., Greber U.F. Adenovirus endocytosis. J. Gene. Med. 2004, 6(Suppl. 1):S152-63.
32. Mosso C., Galvan-Mendoza I.J., Ludert J.E., del Angel R.M. Endocytic pathway followed by dengue virus to infect the mosquito cell line C6/36 HT. Virology 2008, 378(1):193-199.
33. Mousavi S.A., Malerod L., Berg T., Kjeken R. Clathrin-dependent endocytosis. Biochem. J. 2004, 377(Pt 1):1-16.
34. Ongvarrasopone C., Chanasakulniyom M., Sritunyalucksana K., Panyim S. Suppression of PmRab7 by dsRNA inhibits WSSV or YHV infection in shrimp. Mar. Biotechnol. (NY) 2008, 10(4):374-381.
35. Pearse B.M. Coated vesicles from pig brain: purification and biochemical characterization. J. Mol. Biol. 1975, 97(1):93-98.
36. Pearse B.M. Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles. Proc. Natl. Acad. Sci. USA 1976, 73(4):1255-1259.
37. Pearse B.M. On the structural and functional components of coated vesicles. J. Mol. Biol. 1978, 126(4):803-812.
38. Pongsomboon S., Tang S., Boonda S., Aoki T., Hirono I., Tassanakajon A. A cDNA microarray approach for analyzing transcriptional changes in Penaeus monodon after infection by pathogens. Fish Shellfish Immunol. 2011, 30(1):439-446.
39. Rapoport I., Chen Y.C., Cupers P., Shoelson S.E., Kirchhausen T. Dileucine-based sorting signals bind to the beta chain of AP-1 at a site distinct and regulated differently from the tyrosine-based motif-binding site. EMBO J. 1998, 17(8):2148-2155.
40. Robinson M.S. 100-kD coated vesicle proteins: molecular heterogeneity and intracellular distribution studied with monoclonal antibodies. J. Cell. Biol. 1987, 104(4):887-895.
41. Schultz J., Milpetz F., Bork P., Ponting C.P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. USA 1998, 95(11):5857-5864.
42. Simmons G., Reeves J.D., Grogan C.C., Vandenberghe L.H., Baribaud F., Whitbeck J.C., Burke E., Buchmeier M.J., Soilleux E.J., Riley J.L., Doms R.W., Bates P., Pohlmann S. DC-SIGN and DC-SIGNR bind Ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology 2003, 305(1):115-123.
43. Simmons G., Rennekamp A.J., Chai N., Vandenberghe L.H., Riley J.L., Bates P. Folate receptor alpha and caveolae are not required for Ebola virus glycoprotein-mediated viral infection. J. Virol. 2003, 77(24):13433-13438.
44. Sittidilokratna N., Dangtip S., Cowley J.A., Walker P.J. RNA transcription analysis and completion of the genome sequence of yellow head nidovirus. Virus Res. 2008, 136(1-2):157-165.
45. Soowannayan C., Flegel F.W., Sithigorngul P., Slater J., Hyatt A., Cramerri S., Wise T., Crane M.S., Cowley J.A., McCulloch R.J., Walker P.J. Detection and differentiation of yellow head complex viruses using monoclonal antibodies. Dis. Aquat. Organ. 2003, 57(3):193-200.
46. Spann K.M., Donaldson R.A., Cowley J.A., walker P.J., Lester R.J.G. Differences in the susceptibility of some penaeid prawn species to gill-associated virus (GAV) infection. Dis. Aquat. Organ. 2000, 4:221-225.
47. Spann K.M., McCulloch R.J., Cowley J.A., East I.J., Walker P.J. Detection of gill-associated virus (GAV) by in situ hybridization during acute and chronic infections of Penaeus monodon and P. esculentus. Dis. Aquat. Organ. 2003, 56:1-10.
48. Suzuki T., Takahashi T., Guo C.T., Hidari K.I., Miyamoto D., Goto H., Kawaoka Y., Suzuki Y. Sialidase activity of influenza A virus in an endocytic pathway enhances viral replication. J. Virol. 2005, 79(18):11705-11715.
49. Tassaneetrithep B., Burgess T.H., Granelli-Piperno A., Trumpfheller C., Finke J., Sun W., Eller M.A., Pattanapanyasat K., Sarasombath S., Birx D.L., Steinman R.M., Schlesinger S., Marovich M.A. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 2003, 197(7):823-829.
50. Ungewickell E., Branton D. Assembly units of clathrin coats. Nature 1981, 289(5796):420-422.
51. Ungewickell E.J., Hinrichsen L. Endocytosis: clathrin-mediated membrane budding. Curr. Opin. Cell. Biol. 2007, 19(4):417-425.
52. Vonderheit A., Helenius A. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 2005, 3(7):e233.
53. Walker P.J., Bonami J.R., Boonsaeng V., Chang P.S., Cowley J.A., Enjuanes L., Flegel T.W., Lightner D.V., Loh P.C., Snijder E.J., Tang K. Family roniviridae. Virus Taxonomy, VIIIth Report of the ICTV 2005, Elsevier, Academic Press, London. C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball (Eds.).
54. Wang C.S., Tang K.J., Kuo G.H., Chen S.N. Yellowhead disease-like virus infection in the kuruma shrimp Penaeus japonicus cultured in Taiwan. Fish Pathol. 1996, 31:177-182.
55. Wijegoonawardane P.K., Cowley J.A., Phan T., Hodgson R.A., Nielsen L., Kiatpathomchai W., Walker P.J. Genetic diversity in the yellow head nidovirus complex. Virology 2008, 380(2):213-225.
56. Wongteerasupaya C., Sriurairatana T., Vickers J.E., Anutara A., Boonsaeng V., Panyim S., Tassanakajon A., Withyachumnarnkul B., Flegel T.W. Yellowhead virus of Penaeus monodon is an RNA virus. Dis. Aquat. Organ. 1995, 22:45-50.